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Article(id=1292765504536601239, tenantId=1146029695717560320, journalId=1291416979304972313, issueId=1291824268032110598, articleNumber=null, orderNo=null, doi=10.3969/j.issn.1005-4847.2026.03.009, pmid=null, cstr=null, oa=null, hot=null, price=null, onlineType=0, articleFormat=0, articleType=null, articleTypeStr=null, receivedDate=1755014400000, receivedDateStr=2025-08-13, revisedDate=null, revisedDateStr=null, acceptedDate=null, acceptedDateStr=null, onlineDate=1786148914702, onlineDateStr=2026-08-08, pubDate=1774800000000, pubDateStr=2026-03-30, doiRegisterDate=null, doiRegisterDateStr=null, onlineIssueDate=1786148914702, onlineIssueDateStr=2026-08-08, onlineJustAcceptDate=null, onlineJustAcceptDateStr=null, onlineFirstDate=null, onlineFirstDateStr=null, sourceXml=null, magXml=null, createTime=1786148914702, creator=13701087609, updateTime=1786148914702, updator=13701087609, issue=Issue{id=1291824268032110598, tenantId=1146029695717560320, journalId=1291416979304972313, year='2026', volume='34', issue='3', pageStart='313', pageEnd='468', issueExtLink='null', onlineDate='null', pubDate='1774800000000', pubDateStr='2026-03-30', beforeIssueId=null, nextIssueId=null, price=null, status=1, issueComplete=1, articleOrder=1, issueType=1, specialIssue=null, createTime=1785924506432, creator='ztmeta', updateTime=1786331936953, updator='13701087609', preIssue=null, nextIssue=null, articleTotal=null, ext={EN=IssueExt(id=1293533155567366441, tenantId=1146029695717560320, journalId=1291416979304972313, issueId=1291824268032110598, language=EN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=), CN=IssueExt(id=1293533155567366442, tenantId=1146029695717560320, journalId=1291416979304972313, issueId=1291824268032110598, language=CN, specialIssueTitle=, coverIllustrator=null, specialIssueEditor=, specialIssueAbout=)}, issueFiles=null, downloadFileDto=null}, startPage=411, endPage=423, ext={EN=ArticleExt(id=1292765504784065176, articleId=1292765504536601239, tenantId=1146029695717560320, journalId=1291416979304972313, language=EN, title=Renal injury and its potential mechanisms in a murine model of non-alcoholic steatohepatitis-associated hepatocellular carcinoma, columnId=null, journalTitle=Acta Laboratorium Animalis Scientia Sinica, columnName=null, runingTitle=null, highlight=null, articleAbstract=
Objective

To investigate renal injury, functional impairment, histopathological characteristics, and molecular features accompanying HCC development in the context of non-alcoholic steatohepatitis, utilizing a novel MASH-HCC murine model (HRAS-HCC). This research seeks to elucidate the underlying mechanisms of MASH-HCC-induced renal injury, thereby providing an essential model tool for clinical investigations into disease pathogenesis and the exploration of diagnostic and therapeutic strategies.

Methods

HRAS-HCC transgenic mice generated in-house were employed, with littermate negative controls and wild-type C57BL/6 mice as comparators. At 5 weeks of age, tamoxifen was administered to induce hepatocyte-specific HRAS expression, thereby initiating and propagating MASH-HCC. Body mass, general condition, and behavioral parameters were monitored serially during disease progression (weeks 1 ~ 4). Blood was collected at predetermined time points for biochemical analyses. Structural and fibrotic changes in renal tissue were evaluated by hematoxylin-eosin(HE) and Masson staining.

Results

Compared with the HRASNON-TAM group, Within 4 weeks, HRAS-HCC mice transitioned from MASH through hepatic fibrosis to established HCC, manifesting jaundice, tachypnea, kyphosis, hematochezia, hepatosplenomegaly, and other clinical signs. At week 4, serum alkaline phosphatase(ALP) was significantly decreased (P < 0.05), whereas blood urea nitrogen(UREA), uric acid(UC), and creatinine(CREA) were markedly elevated (P < 0.05). HE staining revealed temporally heterogeneous renal lesions, including tubular basophilia, hyaline glomerulopathy, and tubular epithelial cytoplasmic hyaline droplet formation. Masson staining demonstrated renal fibrosis whose onset (weeks 2 ~ 3) and severity paralleled those of hepatic fibrosis/cirrhosis(weeks 2 ~ 3). Further analysis of kidney injury-related molecular expression revealed at week 3 showed up-regulation of keratin-18, SMAD3, fibronectin, and transforming growth factor-β mRNAs (P < 0.05). Protein-protein interaction analyses further indicated direct interactions among human HRAS, fibronectin (FN1), and SMAD3.

Conclusions

These data establish a positive correlation between MASH HCC-induced renal injury and the degree of hepatic fibrosis, clarify the attendant histopathological and molecular signatures, and implicate the HRAS-SMAD3-FN1 axis as a putative mechanistic pathway. The HRAS-HCC mouse model uniquely recapitulates key clinicopathological features of human MASH-HCC complicated by CKD, thereby providing a robust pre-clinical platform for mechanistic dissection and therapeutic development.

, authors=Weijia LI1, 2, Chen LING2, Guitao HUO3, Yanwei YANG3, Susu LIU2, Haoyang ZHAO2, Yining WANG2, Sihao WANG1, 2, Xialu WANG1, *, Changfa FAN2, *, authorsList=Weijia LI, Chen LING, Guitao HUO, Yanwei YANG, Susu LIU, Haoyang ZHAO, Yining WANG, Sihao WANG, Xialu WANG, Changfa FAN, authorCompany=null, correspAuthors=Xialu WANG, Changfa FAN, authorNote=null, correspAuthorsNote=
FAN Changfa. E-mail:
WANG Xialu. E-mail:
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目的

本研究拟基于新型非酒精性脂肪性肝炎（metabolic dysfunction-associated steatohepatitis, MASH）-肝细胞癌（hepatocellular carcinoma, HCC）小鼠模型（HRAS-HCC），研究伴随非酒精性脂肪肝炎相关的肝癌发生的肾损伤、功能失调、组织学及分子学特征，以探索MASH-HCC诱发肾损伤的潜在机制，旨在为临床研究疾病发生机制及探索诊疗方法提供重要模型工具。

方法

实验采用本课题组自主构建的HRAS-HCC小鼠，以同窝隐性小鼠和野生型C57BL/6小鼠为对照组。5周龄时通过注射他莫西芬诱导小鼠肝组织中HRAS基因表达，进而引发MASH-HCC的发生与进展。在MASH-HCC进展过程中（1 ~ 4周），定期监测小鼠的体质量、精神状态等一般特征，并于选择时间点采集血液样本并检测相关指标；通过苏木素-伊红（HE）和Masson染色分析小鼠肾组织的病变特征。

结果

与HRASNON-TAM组相比，HRAS-HCC小鼠在一个月内从MASH阶段，经肝纤维化进展到HCC，表现出黄疸、呼吸急促、弓背、便血、肝肿大和脾肿大等临床症状。4周时，HRAS-HCC小鼠血清中碱性磷酸酶（ALP）降低（P < 0.05），血清尿酸氮（UREA）、尿酸（UA）和肌酐（CREA）升高（P< 0.05）。HE结果显示，HRAS-HCC小鼠肾组织在不同时期存在程度不一的肾小管嗜碱性变、透明性肾小球、肾小管上皮细胞透明滴样变等多种病变。同时，Masson染色观察到HRAS-HCC小鼠肾组织还存在纤维化病变，且肾纤维化（2 ~ 3周）与肝纤维化/肝硬化（2 ~ 3周）的发生时间及严重程度存在相关性。进一步检测肾损伤相关分子表达发现，3周时细胞角蛋白18（KRT18）、SMAD3、纤维连接蛋白1（FN1）、转化生长因子β（TGFβ）在mRNA水平表达升高（P < 0.05）。同时，蛋白质互作网络（PPI）分析结果显示人源HRAS和FN1、SMAD3间存在蛋白互作关系。

结论

本研究结果表明，MASH-HCC引起的肾损伤与肝纤维化程度呈正相关关系，初步展示了MASH-HCC引起的肾损伤病理特征和分子特征，提示HRAS-SMAD3-FN1轴可能存在重要的作用。本研究呈现了特有的MASH-HCC伴随肾损伤动物模型，该模型较真实的重现了临床上肾损伤的疾病特征，为制定该疾病的临床治疗策略奠定了基础。

, authors=李维佳1, 2, 凌晨2, 霍桂桃3, 杨艳伟3, 刘甦苏2, 赵皓阳2, 王依宁2, 王思浩1, 2, 王夏璐1, *, 范昌发2, *, authorsList=李维佳, 凌晨, 霍桂桃, 杨艳伟, 刘甦苏, 赵皓阳, 王依宁, 王思浩, 王夏璐, 范昌发, authorCompany=null, correspAuthors=王夏璐, 范昌发, authorNote=

# 共同第一作者

* 共同通信作者

李维佳，男，在读硕士研究生，研究方向：疾病动物模型。Email：

凌晨，女，博士，研究方向：疾病动物模型。Email：。

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范昌发，男，博士，研究员，博士生导师，研究方向：疾病动物模型。Email：
王夏璐，女，博士，副教授，研究方向：生物诊断试剂开发。Email：。
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2．中国食品药品检定研究院实验动物资源研究所（国家啮齿类实验动物资源库），北京　102629, bio={"content":"

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非酒精性脂肪性肝炎相关肝细胞癌进展中小鼠肾损伤程度及其潜在机制研究
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李维佳 1, 2 , 凌晨 2 , 霍桂桃 3 , 杨艳伟 3 , 刘甦苏 2 , 赵皓阳 2 , 王依宁 2 , 王思浩 1, 2 , 王夏璐 1, * , 范昌发 2, *
中国实验动物学报 | 研究报告 2026,34(3): 411-423
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中国实验动物学报 |研究报告 2026 , 34 (3) : 411 -423
非酒精性脂肪性肝炎相关肝细胞癌进展中小鼠肾损伤程度及其潜在机制研究
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李维佳1, 2 , 凌晨2 , 霍桂桃3, 杨艳伟3, 刘甦苏2, 赵皓阳2, 王依宁2, 王思浩1, 2, 王夏璐1, * , 范昌发2, *
作者信息
  • 1．沈阳药科大学，沈阳　110016
  • 2．中国食品药品检定研究院实验动物资源研究所（国家啮齿类实验动物资源库），北京　102629
  • 3．中国食品药品检定研究院安全评价研究所（国家药物安全评价检测中心，北京　100176
通讯作者:
范昌发，男，博士，研究员，博士生导师，研究方向：疾病动物模型。Email：
王夏璐，女，博士，副教授，研究方向：生物诊断试剂开发。Email：。
作者简介:

# 共同第一作者

* 共同通信作者

李维佳，男，在读硕士研究生，研究方向：疾病动物模型。Email：

凌晨，女，博士，研究方向：疾病动物模型。Email：。

Renal injury and its potential mechanisms in a murine model of non-alcoholic steatohepatitis-associated hepatocellular carcinoma
Weijia LI1, 2 , Chen LING2 , Guitao HUO3, Yanwei YANG3, Susu LIU2, Haoyang ZHAO2, Yining WANG2, Sihao WANG1, 2, Xialu WANG1, * , Changfa FAN2, *
Affiliations
  • 1.Shenyang Pharmaceutical University, Shenyang 110016, China
  • 2.Institute for Laboratory Animal Resources, National Institutes for Food and Drug Control (National Rodent Laboratory Animal Resource Bank), Beijing 102629, China
  • 3.Institute for Safety Evaluation, National Institutes for Food and Drug Control (National Center for Safety Evaluation of Drugs, Beijing 100176, China
    • Corresponding Author:
    FAN Changfa. E-mail:
    WANG Xialu. E-mail:
出版时间: 2026-03-30 doi: 10.3969/j.issn.1005-4847.2026.03.009
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摘要
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目的

本研究拟基于新型非酒精性脂肪性肝炎（metabolic dysfunction-associated steatohepatitis, MASH）-肝细胞癌（hepatocellular carcinoma, HCC）小鼠模型（HRAS-HCC），研究伴随非酒精性脂肪肝炎相关的肝癌发生的肾损伤、功能失调、组织学及分子学特征，以探索MASH-HCC诱发肾损伤的潜在机制，旨在为临床研究疾病发生机制及探索诊疗方法提供重要模型工具。

方法

实验采用本课题组自主构建的HRAS-HCC小鼠，以同窝隐性小鼠和野生型C57BL/6小鼠为对照组。5周龄时通过注射他莫西芬诱导小鼠肝组织中HRAS基因表达，进而引发MASH-HCC的发生与进展。在MASH-HCC进展过程中（1 ~ 4周），定期监测小鼠的体质量、精神状态等一般特征，并于选择时间点采集血液样本并检测相关指标；通过苏木素-伊红（HE）和Masson染色分析小鼠肾组织的病变特征。

结果

与HRASNON-TAM组相比，HRAS-HCC小鼠在一个月内从MASH阶段，经肝纤维化进展到HCC，表现出黄疸、呼吸急促、弓背、便血、肝肿大和脾肿大等临床症状。4周时，HRAS-HCC小鼠血清中碱性磷酸酶（ALP）降低（P < 0.05），血清尿酸氮（UREA）、尿酸（UA）和肌酐（CREA）升高（P< 0.05）。HE结果显示，HRAS-HCC小鼠肾组织在不同时期存在程度不一的肾小管嗜碱性变、透明性肾小球、肾小管上皮细胞透明滴样变等多种病变。同时，Masson染色观察到HRAS-HCC小鼠肾组织还存在纤维化病变，且肾纤维化（2 ~ 3周）与肝纤维化/肝硬化（2 ~ 3周）的发生时间及严重程度存在相关性。进一步检测肾损伤相关分子表达发现，3周时细胞角蛋白18（KRT18）、SMAD3、纤维连接蛋白1（FN1）、转化生长因子β（TGFβ）在mRNA水平表达升高（P < 0.05）。同时，蛋白质互作网络（PPI）分析结果显示人源HRAS和FN1、SMAD3间存在蛋白互作关系。

结论

本研究结果表明，MASH-HCC引起的肾损伤与肝纤维化程度呈正相关关系，初步展示了MASH-HCC引起的肾损伤病理特征和分子特征，提示HRAS-SMAD3-FN1轴可能存在重要的作用。本研究呈现了特有的MASH-HCC伴随肾损伤动物模型，该模型较真实的重现了临床上肾损伤的疾病特征，为制定该疾病的临床治疗策略奠定了基础。

代谢障碍相关脂肪性肝炎  /  肝细胞癌  /  HRAS  /  肾损伤  /  小鼠模型
Objective

To investigate renal injury, functional impairment, histopathological characteristics, and molecular features accompanying HCC development in the context of non-alcoholic steatohepatitis, utilizing a novel MASH-HCC murine model (HRAS-HCC). This research seeks to elucidate the underlying mechanisms of MASH-HCC-induced renal injury, thereby providing an essential model tool for clinical investigations into disease pathogenesis and the exploration of diagnostic and therapeutic strategies.

Methods

HRAS-HCC transgenic mice generated in-house were employed, with littermate negative controls and wild-type C57BL/6 mice as comparators. At 5 weeks of age, tamoxifen was administered to induce hepatocyte-specific HRAS expression, thereby initiating and propagating MASH-HCC. Body mass, general condition, and behavioral parameters were monitored serially during disease progression (weeks 1 ~ 4). Blood was collected at predetermined time points for biochemical analyses. Structural and fibrotic changes in renal tissue were evaluated by hematoxylin-eosin(HE) and Masson staining.

Results

Compared with the HRASNON-TAM group, Within 4 weeks, HRAS-HCC mice transitioned from MASH through hepatic fibrosis to established HCC, manifesting jaundice, tachypnea, kyphosis, hematochezia, hepatosplenomegaly, and other clinical signs. At week 4, serum alkaline phosphatase(ALP) was significantly decreased (P < 0.05), whereas blood urea nitrogen(UREA), uric acid(UC), and creatinine(CREA) were markedly elevated (P < 0.05). HE staining revealed temporally heterogeneous renal lesions, including tubular basophilia, hyaline glomerulopathy, and tubular epithelial cytoplasmic hyaline droplet formation. Masson staining demonstrated renal fibrosis whose onset (weeks 2 ~ 3) and severity paralleled those of hepatic fibrosis/cirrhosis(weeks 2 ~ 3). Further analysis of kidney injury-related molecular expression revealed at week 3 showed up-regulation of keratin-18, SMAD3, fibronectin, and transforming growth factor-β mRNAs (P < 0.05). Protein-protein interaction analyses further indicated direct interactions among human HRAS, fibronectin (FN1), and SMAD3.

Conclusions

These data establish a positive correlation between MASH HCC-induced renal injury and the degree of hepatic fibrosis, clarify the attendant histopathological and molecular signatures, and implicate the HRAS-SMAD3-FN1 axis as a putative mechanistic pathway. The HRAS-HCC mouse model uniquely recapitulates key clinicopathological features of human MASH-HCC complicated by CKD, thereby providing a robust pre-clinical platform for mechanistic dissection and therapeutic development.

metabolic dysfunction-associated steatohepatitis  /  hepatocellular carcinoma  /  HRAS  /  renal injury  /  mouse model
李维佳, 凌晨, 霍桂桃, 杨艳伟, 刘甦苏, 赵皓阳, 王依宁, 王思浩, 王夏璐, 范昌发. 非酒精性脂肪性肝炎相关肝细胞癌进展中小鼠肾损伤程度及其潜在机制研究. 中国实验动物学报, 2026 , 34 (3) : 411 -423 . DOI: 10.3969/j.issn.1005-4847.2026.03.009
Weijia LI, Chen LING, Guitao HUO, Yanwei YANG, Susu LIU, Haoyang ZHAO, Yining WANG, Sihao WANG, Xialu WANG, Changfa FAN. Renal injury and its potential mechanisms in a murine model of non-alcoholic steatohepatitis-associated hepatocellular carcinoma[J]. Acta Laboratorium Animalis Scientia Sinica, 2026 , 34 (3) : 411 -423 . DOI: 10.3969/j.issn.1005-4847.2026.03.009
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  • 中国食品药品检定研究院关键技术研究基金课题(GJJSYJ202401)
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doi: 10.3969/j.issn.1005-4847.2026.03.009
  • 接收时间：2025-08-13
  • 首发时间：2026-08-08
  • 出版时间：2026-03-30
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  • 收稿日期：2025-08-13
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Key Technology Research Fund Project of the National Institutes for Food and Drug Control(GJJSYJ202401)
中国食品药品检定研究院关键技术研究基金课题(GJJSYJ202401)
作者信息
    1．沈阳药科大学，沈阳　110016
    2．中国食品药品检定研究院实验动物资源研究所（国家啮齿类实验动物资源库），北京　102629
    3．中国食品药品检定研究院安全评价研究所（国家药物安全评价检测中心，北京　100176

通讯作者:

范昌发，男，博士，研究员，博士生导师，研究方向：疾病动物模型。Email：
王夏璐，女，博士，副教授，研究方向：生物诊断试剂开发。Email：。
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https://castjournals.cast.org.cn/joweb/zgsydwxb/CN/10.3969/j.issn.1005-4847.2026.03.009
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